In 2005, she defeated incumbent
New Democratic Party Member of Parliament Bev Desjarlais for the NDP nomination due in part to her support of
same-sex marriage after Desjarlais broke party ranks to vote against the
Civil Marriage Act. Desjarlais subsequently quit the party, sat as an
independent for the remainder of her term in the
38th Parliament and ran against Ashton as an independent candidate in the election in the Churchill riding in the
2006 Canadian federal election. The major themes in Ashton's campaign included getting federal funding for the University College of the North and a federal agreement for northern development. Although the labour unions in Thompson endorsed Ashton, the NDP vote nevertheless split between Ashton and Desjarlais, and
Liberal candidate
Tina Keeper won the riding. Ashton defeated Keeper in the
2008 election, regaining the riding for the NDP. On November 7, 2011, in
Montreal, Ashton launched her campaign as the ninth person to join the
2012 NDP leadership race. At the age of 29, she was the youngest of the candidates. She placed seventh with 5.7% of the vote at the March 24, 2012 leadership election and was eliminated on the first ballot. Since first being elected in 2008, Ashton was elected as the Chair of the House of Commons Standing Committee on the Status of Women in the 40th Parliament of Canada. She has also served as the NDP Post-Secondary and Youth critic, as the Rural and Community Development critic and from 2012 to 2014 as the Status of Women Critic. On January 23, 2015, Ashton was appointed as the Aboriginal Affairs Critic in Canada's Official Opposition. After the
2015 federal election, Ashton was appointed the NDP critic for Jobs, Employment and Workforce Development in the
42nd Canadian Parliament. event in 2017 Ashton announced her candidacy for the
2017 NDP leadership election on March 7, 2017. She placed third in the October 1, 2017 election, with 17.4% of the vote, just over 1,000 votes behind runner up
Charlie Angus.
Jagmeet Singh was elected leader on the first ballot. Ashton was re-elected in the 2019 federal election. She was stripped of her critic roles on January 1, 2021, after revealing to the public on
Twitter that she had travelled to Greece during the 2020 COVID-19 second wave to visit an "ailing grandmother." She had not informed party leadership of her travel plans beforehand. She was re-elected in the
2021 federal election. In June 2024, media reports surfaced that Ashton, who frequently joined parliamentary proceedings remotely, billed taxpayers $17,641 for a family trip over Christmas 2022, citing stakeholder meetings on official language priorities. Ashton, her partner, and their children travelled from Thompson, Manitoba, to Ottawa, Quebec City, and Montreal, with some expenses covering leisure activities. After the story was released, Ashton agreed to return $2,900 or 16% of the amounts claimed. Ashton was defeated in the
2025 federal election. ==Political views==